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Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation

BACKGROUND: Carotenoids are important pigments and precursors for central signaling molecules associated in fruit development and ripening. Carotenoid metabolism has been studied especially in the climacteric tomato fruit but the content of carotenoids and the regulation of their metabolism have bee...

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Autores principales: Karppinen, Katja, Zoratti, Laura, Sarala, Marian, Carvalho, Elisabete, Hirsimäki, Jenni, Mentula, Helmi, Martens, Stefan, Häggman, Hely, Jaakola, Laura
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4839083/
https://www.ncbi.nlm.nih.gov/pubmed/27098458
http://dx.doi.org/10.1186/s12870-016-0785-5
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author Karppinen, Katja
Zoratti, Laura
Sarala, Marian
Carvalho, Elisabete
Hirsimäki, Jenni
Mentula, Helmi
Martens, Stefan
Häggman, Hely
Jaakola, Laura
author_facet Karppinen, Katja
Zoratti, Laura
Sarala, Marian
Carvalho, Elisabete
Hirsimäki, Jenni
Mentula, Helmi
Martens, Stefan
Häggman, Hely
Jaakola, Laura
author_sort Karppinen, Katja
collection PubMed
description BACKGROUND: Carotenoids are important pigments and precursors for central signaling molecules associated in fruit development and ripening. Carotenoid metabolism has been studied especially in the climacteric tomato fruit but the content of carotenoids and the regulation of their metabolism have been shown to be highly variable between fruit species. Non-climacteric berries of the genus Vaccinium are among the best natural sources of health-beneficial flavonoids but not studied previously for carotenoid biosynthesis. RESULTS: In this study, carotenoid biosynthetic genes, PSY, PDS, ZDS, CRTISO, LCYB, LCYE, BCH and CYP450-BCH, as well as a carotenoid cleavage dioxygenase CCD1 were identified from bilberry (V. myrtillus L.) fruit and their expression was studied along with carotenoid composition during fruit development under different photoperiod and light quality conditions. Bilberry was found to be a good source of carotenoids among fruits and berries. The most abundant carotenoids throughout the berry development were lutein and β-carotene, which were accompanied by lower amounts of 9Z-β-carotene, violaxanthin, neoxanthin, zeaxanthin, antheraxanthin and β-cryptoxanthin. The expression patterns of the biosynthetic genes in ripening fruits indicated a metabolic flux towards β-branch of the carotenoid pathway. However, the carotenoid levels decreased in both the β-branch and ε,β-branch towards bilberry fruit ripening along with increased VmCCD1 expression, similarly to VmNCED1, indicating enzymatic carotenoid cleavage and degradation. Intense white light conditions increased the expression of the carotenoid biosynthetic genes but also the expression of the cleavage genes VmCCD1 and VmNCED1, especially in unripe fruits. Instead, mature bilberry fruits responded specifically to red/far-red light wavelengths by inducing the expression of both the carotenoid biosynthetic and the cleavage genes indicating tissue and developmental stage specific regulation of apocarotenoid formation by light quality. CONCLUSIONS: This is the first report of carotenoid biosynthesis in Vaccinium berries. Our results indicate that both transcriptional regulation of the key biosynthetic genes and the enzymatic degradation of the produced carotenoids to apocarotenoids have significant roles in the determination of the carotenoid content and have overall effect on the metabolism during the bilberry fruit ripening. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0785-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-48390832016-04-22 Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation Karppinen, Katja Zoratti, Laura Sarala, Marian Carvalho, Elisabete Hirsimäki, Jenni Mentula, Helmi Martens, Stefan Häggman, Hely Jaakola, Laura BMC Plant Biol Research Article BACKGROUND: Carotenoids are important pigments and precursors for central signaling molecules associated in fruit development and ripening. Carotenoid metabolism has been studied especially in the climacteric tomato fruit but the content of carotenoids and the regulation of their metabolism have been shown to be highly variable between fruit species. Non-climacteric berries of the genus Vaccinium are among the best natural sources of health-beneficial flavonoids but not studied previously for carotenoid biosynthesis. RESULTS: In this study, carotenoid biosynthetic genes, PSY, PDS, ZDS, CRTISO, LCYB, LCYE, BCH and CYP450-BCH, as well as a carotenoid cleavage dioxygenase CCD1 were identified from bilberry (V. myrtillus L.) fruit and their expression was studied along with carotenoid composition during fruit development under different photoperiod and light quality conditions. Bilberry was found to be a good source of carotenoids among fruits and berries. The most abundant carotenoids throughout the berry development were lutein and β-carotene, which were accompanied by lower amounts of 9Z-β-carotene, violaxanthin, neoxanthin, zeaxanthin, antheraxanthin and β-cryptoxanthin. The expression patterns of the biosynthetic genes in ripening fruits indicated a metabolic flux towards β-branch of the carotenoid pathway. However, the carotenoid levels decreased in both the β-branch and ε,β-branch towards bilberry fruit ripening along with increased VmCCD1 expression, similarly to VmNCED1, indicating enzymatic carotenoid cleavage and degradation. Intense white light conditions increased the expression of the carotenoid biosynthetic genes but also the expression of the cleavage genes VmCCD1 and VmNCED1, especially in unripe fruits. Instead, mature bilberry fruits responded specifically to red/far-red light wavelengths by inducing the expression of both the carotenoid biosynthetic and the cleavage genes indicating tissue and developmental stage specific regulation of apocarotenoid formation by light quality. CONCLUSIONS: This is the first report of carotenoid biosynthesis in Vaccinium berries. Our results indicate that both transcriptional regulation of the key biosynthetic genes and the enzymatic degradation of the produced carotenoids to apocarotenoids have significant roles in the determination of the carotenoid content and have overall effect on the metabolism during the bilberry fruit ripening. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0785-5) contains supplementary material, which is available to authorized users. BioMed Central 2016-04-21 /pmc/articles/PMC4839083/ /pubmed/27098458 http://dx.doi.org/10.1186/s12870-016-0785-5 Text en © Karppinen et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Karppinen, Katja
Zoratti, Laura
Sarala, Marian
Carvalho, Elisabete
Hirsimäki, Jenni
Mentula, Helmi
Martens, Stefan
Häggman, Hely
Jaakola, Laura
Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation
title Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation
title_full Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation
title_fullStr Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation
title_full_unstemmed Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation
title_short Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation
title_sort carotenoid metabolism during bilberry (vaccinium myrtillus l.) fruit development under different light conditions is regulated by biosynthesis and degradation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4839083/
https://www.ncbi.nlm.nih.gov/pubmed/27098458
http://dx.doi.org/10.1186/s12870-016-0785-5
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